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Ivan Chernyakhovsky was born in 1906. His father was a railwayman who died of typhus when his son was nine. He was a railway worker until joining the Red Army in 1924. In 1928 he finished the officer's school in Kiev. Due to the rapid pre-war expansion of the RKKA and 1937–1938 military purges, he quickly rose in rank. In 1938 he became commander of the 9th Light Tank Brigade. In March 1941 he became the commander of the 28th Tank Division in the Baltic Military District. In July 1942 promoted to the commander of the 18th Tank Corps defending Voronezh.

On 8 February 1943, elements of Chernyakhovsky's 60th Army hoisted a victorious Red Banner over the city of Kursk after a fast advance to the city from Voronezh, which was retaken some two weeks before.

Operation Bagration was launched after a four month break in activities because of the spring thaw. The Soviets launched their attack on June 22 on four fronts with 146 infantry and 43 armored divisions. General Bagramyan's 1st Baltic Front and General Chernyakhovsky's 3rd Belorussian Front struck to the north and south of Vitebsk and took the city on June 27. Chernyakhovsky's left wing then took Orsha – this meant that the Moscow–Minsk highway could now be used to threaten the German rear. To the south, General Zakharov's 2nd Belorussian Front, north of the Pripet Marshes, destroyed a force of 33,000 at Babruysk on that day. Chernyakhovsky's army now headed for Minsk. On July 2 his mobile forces reached Stolbtsy, 40 miles away. General Rotmistrov's tanks entered Minsk on 3 July and 50,000 Germans were trapped.

The offensive pressed on to Baranavichy (8 July) and to Hrodna (13 July). In the south Rokossovsky cleared the Pripet Marshes taking Pinsk and Kovel on 5 July. In the north Bagramyan turned to the Baltic States and took Vilnius in Lithuania and Daugavpils in Latvia on 13 July. This split the Army Group North in two (East Prussia and the Baltic States). The Soviets arrived on the Polish border within 24 days and claimed to had taken 158,000 men, 2,000 tanks, 10,000 guns, and 57,000 motor vehicles. They also claimed to have killed 38,000 Germans. It was a resounding defeat for the Germans and Hitler dismissed Busch from the command of Army Group Centre, replacing him with Model. The Soviets had swept the Germans from Belorussia by mid-July 1944 and they pressed their advantage by attacking Poland. In the north Generals Chernyakhovsky and Zakharov joined to take Białystok on 18 July.

In summer 1944 General Chernyakhovsky pressed the Germans on the frontiers of their own land in East Prussia. His 3rd Belorussian Front drove across the Neman River, taking Kaunas on 1 August, and pressed the eastern border of East Prussia. The center thrust took Suwalki on July 26 and General Bagramyan occupied the Tukums junction on the Gulf of Riga.

Prior to his death in 1945, Chernyakhovsky launched the Soviet East Prussian Offensive against stiff resistance from the III Panzer Army. He was part of the drive on Berlin. Together with Marshal Konstantin Rokossovsky's 2nd Belorussian Front, which attacked East Prussia from the south and then headed north-westwards towards the Baltic coast around Danzig (Gdańsk), the 3rd Belorussian Front, commanded by General Chernyakhovsky was ordered to attack from the east towards Königsberg, even though this meant throwing his armies against heavy German defence works. These two fronts mustered 1,670,000 men with 28,360 guns and heavy mortars and 3,300 tanks.

Marshal Rokossovsky's front made contact with Marshal Zhukov's forces at Grudziadz (German: Graudenz) and they wheeled north towards Danzig to cut off East Prussia. More than 500,000 Germans were caught in a pocket, but many were evacuated. On 10 February, Rokossovsky reached the coast near Elbing (Elbląg) and East Prussia was under siege from the south and east by the 3rd Byelorussian Front.

From January 1945 until February 18, 1945, Chernyakhovsky was appointed Soviet supreme commander of East Prussia.

On 1 February Chernyakhovsky split the pocket by attacking between Elbing and Königsberg. Just over 2 weeks later, on February 18, Chernyakhovsky, the youngest front commander of World War II, was killed by shell fragments from artillery fire while inspecting preparations for an offensive.

Chernyakhovsky was buried in Vilnius, Lithuania, near a square named in his honor. After Lithuania declared its independence from the Soviet Union in 1990 and following the dissolution of the Soviet Union itself in 1991, Chernyaknovsky's remains were reburied at the Novodevichy Cemetery in Moscow in 1992. The monument to Chernyakhovsky, dismantled by the authorities of Vilnius, was reinstated in the Russian city of Voronezh that was defended in the fall of 1942 and liberated in January 1943 by the 60th Army under his command.

After World War II, when the Soviet Union annexed northern East Prussia and expelled the Germans, the town of Insterburg was renamed Chernyakhovsk in his honor.